Interdisciplinary interventions that improve patient-reported outcomes in perioperative cancer care: A systematic review of randomized control trials

Introduction Interdisciplinary teams are often leveraged to improve quality of cancer care in the perioperative period. We aimed to identify the team structures and processes in interdisciplinary interventions that improve perioperative patient-reported outcomes for patients with cancer. Methods We searched PubMed, EMBASE, and CINAHL for randomized control trials published at any time and screened 7,195 articles. To be included in our review, studies needed to report patient-reported outcomes, have interventions that occur in the perioperative period, include surgical cancer treatment, and include at least one non physician intervention clinical team member: advanced practice providers, including nurse practitioners and physician assistants, clinical nurse specialists, and registered nurses. We narratively synthesized intervention components, specifically roles assumed by intervention clinical team members and interdisciplinary team processes, to compare interventions that improved patient-reported outcomes, based on minimal clinically important difference and statistical significance. Results We included 34 studies with a total of 4,722 participants, of which 31 reported a clinically meaningful improvement in at least one patient-reported outcome. No included studies had an overall high risk of bias. The common clinical team member roles featured patient education regarding diagnosis, treatment, coping, and pain/symptom management as well as postoperative follow up regarding problems after surgery, resource dissemination, and care planning. Other intervention components included six or more months of continuous clinical team member contact with the patient and involvement of the patient’s caregiver. Conclusions Future interventions might prioritize supporting clinical team members roles to include patient education, caregiver engagement, and clinical follow-up.


Introduction
Interdisciplinary teams are often leveraged to improve quality of cancer care in the perioperative period.We aimed to identify the team structures and processes in interdisciplinary interventions that improve perioperative patient-reported outcomes for patients with cancer.

Methods
We searched PubMed, EMBASE, and CINAHL for randomized control trials published at any time and screened 7,195 articles.To be included in our review, studies needed to report patient-reported outcomes, have interventions that occur in the perioperative period, include surgical cancer treatment, and include at least one non physician intervention clinical team member: advanced practice providers, including nurse practitioners and physician assistants, clinical nurse specialists, and registered nurses.We narratively synthesized intervention components, specifically roles assumed by intervention clinical team members and interdisciplinary team processes, to compare interventions that improved patient-reported outcomes, based on minimal clinically important difference and statistical significance.

Results
We included 34 studies with a total of 4,722 participants, of which 31 reported a clinically meaningful improvement in at least one patient-reported outcome.No included studies had

Introduction
Teams play an important role in fostering better care for patients with serious conditions or when treatment is complex [1].A team can be either bounded, where members have static, defined roles, or dynamic, where members adjust roles continuously based on the task [2,3].Traditionally, nurses and physicians had their own individual roles when treating patients, and their responsibilities did not overlap or change frequently while treating a patient [2].The dynamic model of teaming is important in healthcare due to the dynamic nature of patient disease trajectories and medical care generally, allowing different members of the healthcare team to adjust their roles as needed to best take care of the patient [4,5].Since physicians often face time constraints when caring for patients, interdisciplinary teams also engage with patients and families to address care needs [6,7].Interdisciplinary teams can be defined as a team that synthesizes and harmonizes links between each individual discipline into a coordinated and coherent whole [8].Leveraging non-physician clinical team members (e.g.advanced practice providers, clinical nurse specialists, and registered nurses) to participate on interdisciplinary teams can improve the quality of life for patients, especially in the context of cancer care [9][10][11].
Both cancer and its treatment often impairs aspects of quality of life (e.g.physical, emotional, existential, and social); because patient needs fluctuate over time, an interdisciplinary team can be leveraged to support patients' changing needs so that the care is customized for each patient [5,[10][11].Recent interventions in perioperative cancer care have revolved around integrating interdisciplinary teams to improve patient education, follow-up, and rehabilitation, leading to improved patient outcomes [10].For example, in a randomized control trial where a nurse practitioner joined the oncology team to discuss hospice, living wills, and advanced directives with patients metastatic cancer, there was an improvement in the patients' quality of life, overall physical, mental, and emotional wellbeing [11].Developing opportunities to improve the quality of life for patients with cancer is particularly important because the symptoms of cancer, as well as the treatment, such as surgery, chemotherapy, or radiation therapy, can severely diminish a patient's quality of life [12].Although surgery can help treat cancer and alleviate symptoms, surgery itself can lead to adverse side effects such as loss of function, pain, and fatigue [13].Improving the quality of life of patients with cancer is important, both due to the adverse effects of cancer, and its treatment.
The perioperative period is an exemplary context in which teams may play an important role in fostering better outcomes in cancer care [14,15].During the perioperative period, surgeons and surgical teams have many complex tasks which require interdisciplinary collaboration: (1) communicate the purpose and expect results of surgery (which may be curative, life-extending, or palliative), (2) identify patients who are appropriate for surgery based on relative risk of frailty or life expectancy, (3) optimize patients for surgery to minimize risks, and (4) quickly identify and manage complications postoperatively [15][16][17][18].
These tasks are critical to complete during the perioperative period since frailty, which is highly prevalent in the cancer population, can be associated with increased postoperative morbidity and mortality, which is an indicator of poor quality of care [17,18].The risks faced by surgical cancer patients over time is underscored by the fact that over 20% of cancer patients over the age of 70 die within 5 years of surgery [12].Since there is an increased incidence of morbidity and mortality in the perioperative period of cancer care, there is an opportunity for leveraging diverse clinical team members to improve outcomes for patients within this time period [10,[18][19][20].
Through this systematic review, we sought to understand how clinical team members might improve perioperative care and how their roles might be further modified or extended to improve perioperative care quality.Despite a recent surge in interventions integrating interdisciplinary teams in perioperative cancer care, individual components of interventions, such as specific structures and processes have not been analyzed.The purpose of this paper was to identify the structures (who is on the team and what are their roles) and processes (how the team functions and communicates) in existing interdisciplinary interventions that improved perioperative patient reported outcomes (PROs) among patients with cancer in randomized controlled trials to garner insights on how future interventions might improve PROs in perioperative cancer care.We also aimed to understand the various components of interventions and the impact they had on PROs.This includes the types of interventions, specific team member roles, and caregiver involvement.

Methods
We used the Preferred Reporting Items for Systematic Reviews and Meta-Analysis Protocols (PRISMA-P) Statement and EQUATOR guidelines to guide the creation of this protocol [21,22].We registered this study protocol to the PROSPERO database under the registration number CRD42021270688 [23].We aimed to identify the structures and processes in interdisciplinary interventions that improve perioperative PROs in randomized controlled trials for patients with cancer.For this paper, we define the non-physician clinical team members as advanced practice providers, clinical nurse specialists, and registered nurses.PROs of interest included the Quality of Life Scales (QLQ-c30), Hospital Anxiety and Depression Scales (HADS), Symptom Distress Scale (SDS), 12-Item Short Form Health Survey (SF-12), Functional Assessment of Cancer Therapy (FACT-C), Functional Assessment of Cancer Therapy (FACT-B), Self-rating Anxiety Scale (SAS), Self-rating Depression Scale (SDS), Profile of Mood States, Gracely Pain Scale, Center for Epidemiologic Studies Depression Scale, Stoma Self-Efficacy Scale, Numerical Rating Scale for pain intensity, American Pain Society-patient questionnaire, and the Mood Adjective Check List (MACL).These metrics help us better understand the impact of interventions on a person's life.

Study selection
To search for the articles that fit the scope of this study, we consulted a professional research librarian (HW).Key concepts included in the search strategy included randomized control trials, cancer care, and clinical team members as shown in Appendix S1 (S1 File).We searched PubMed, Embase, and CINAHL in June 2021 and again to update the search in March 2023 for studies published at any time and ended up with 11,222 articles (8,020 articles after duplicates were removed).Inclusion criteria were: RCTs, adults (18 and over), English only (for feasibility), PROs, inclusion of clinical team members as part of the healthcare team, perioperative period (defined as 30 days before and up to 90 days after surgery), and cancer care in the in-patient or out-patient/ ambulatory setting [15].Exclusion criteria were: non-RCTs, protocol papers, pediatric population, studies not written in English, no PROs, no clinical team member in the intervention, not during the perioperative period, no patients with cancer, or interventions testing the technical execution of surgery, radiation, pharmaceutical delivery, or other clinical therapies.
We also excluded studies of art/music therapy, exercise therapy, diet changes, or spiritual therapy for patients because these interventions have been extensively studied in the literature as effective programs on their own.These represent specific clinical interventions that have been shown to be effective on their own, regardless of what team members facilitating the intervention, and we wanted this systematic review to focus on the components of interventions (e.g.team structure and processes) that impacted PROs [24][25][26].The eligibility criteria are detailed through the population, intervention, comparator, outcomes, timing, and setting (PICOTS) framework as shown by Table 1.
During the title/abstract screening and full-text screening phases, two reviewers evaluated each study and were blinded to each other's decisions (BM and SF).During the title/abstract screening (inter-rater reliability; Cohen's Kappa = 0.94022), we resolved all conflicts by a group consensus or by a "gold standard" reviewer (KG).We screened the full texts that remained after the title/abstract screening in a similar way.During the full-text screening (inter-rater reliability; Cohen's Kappa = 0.84632), the reason for exclusion was also identified.Only the "gold standard" reviewer resolved conflicts during the full-text screening phase (KG).We used the Covidence software to generate a PRISMA diagram to track the studies at each stage of the review [27].During this process, if any systematic reviews met our inclusion criteria, we added their references lists to the title/abstract screening process.We then rejected these systematic reviews that met inclusion criteria, but kept any additional articles gained through screening of the reference lists.

Population Inclusion
• Adult patients receiving cancer care in the perioperative period in both the control and treatment groups.

Exclusion
• Studies that include pediatric/ adolescent patients.

Intervention Inclusion:
• We will include studies that have a clinical team member that is trained for the study and provides the intervention for the patient.
� This includes advanced practice providers, clinical nurse specialists, or registered nurses.
■ Advanced practice providers include physician assistants, nurse practitioners, certified nurse midwives, and certified registered nurse anesthetists.

Exclusion
• All studies exclusively examining the technical execution of surgery, radiation, or pharmaceutical delivery itself will not be included in the study.
• All studies exclusively examining the technical execution of art/music therapy, exercise therapy, diet changes, or spiritual therapy will be excluded.

Comparator
• Usual care

Outcomes
• Any patient reported outcomes

Timing
• Interventions with any follow-up period will be included.

Setting
• Any care setting (including in-person surgical clinics or out-patient/ ambulatory care) as long as the intervention encompasses the surgical team and perioperative care.https://doi.org/10.1371/journal.pone.0294599.t001

Data collection
During the screening process, we built an abstraction form through an iterative process which included palliative care physicians (NS, KL, and SD) as well as practicing urologists (JB and JL).All parts of the intervention were recorded, including what the intervention entailed, the roles of the clinical team members, team structures, team processes, and the extent of caregiver involvement.To expand upon the current knowledge of team based interventions, the definition of teamwork was broadened to include teaming.In the search strategy, "team" or "teamwork" or "teaming" was not used as a limiting term since articles that utilize teaming within the healthcare team in the intervention might not explicitly mention these words.To ensure the processes by which teaming occurred in the intervention was collected, the creation of the abstraction guide was informed by the broadened definition.In the abstraction guide, the definition for teaming used was at least two clinicians interacting with each other and with patients over at least two distinct timepoints [28].
The main outcomes collected were any form of PROs.PROs in the perioperative period can be used to quantitatively assess a patient's quality of life [29].Healthcare teams can utilize PROs as tools to improve patient outcomes, inform best practices, and refine patient care [30].Through different patient-reported outcomes (such as the Functional Assessment of Cancer Therapy Scale, QLQ-c30, Profile of Mood States, MACL, HADS), researchers can understand how study interventions may impact patient quality of life [29].
Additional outcomes we collected were evidence of family involvement in decision making, whether the intervention took place during the perioperative period (defined as 30 days before and up to 90 days after surgery) [16].The entire abstraction guide is shown in Appendix S2 (S1 File).Data abstraction for the included studies was done similar to the screening process in which two reviewers (BM, NS, or SF) abstracted each article independently and resolved all conflicts through a consensus conversation.Risk assessment for bias (Appendix S3 in S1 File) was also done in the same way using the Cochrane Risk of Bias tool for randomized control trials [31].The Cochrane Risk of Bias tool is an accepted risk of bias assessment for RCTs and considered seven domains: sequence generation, allocation concealment.blinding of participants and personnel, blinding of outcome assessors, incomplete outcome data, selective outcome reporting, and other sources of bias [31].

Data synthesis
We performed a narrative synthesis because of the high degree of heterogeneity stemming from the different forms of PROs used in the studies.Each included study used different methods, and reported different outcomes, which hinders meaningful statistical pooling.We evaluated both clinically significant differences and statistically significant differences.Specifically, we considered the intervention components and mapped them to clinically meaningful improvement in PROs defined by the minimal clinically important difference (MCID) [29,32].MCID is defined as the smallest possible change in a reported outcome that has a clinical impact [29,32].In studies with PROs that as of yet do not have established MCID, we only considered statistical significance since this was the only reliable metric available to analyze the data from the included studies.The entire intervention description provided was compared to the other intervention descriptions to find similar components across the various interventions.We analyzed the expanded roles of clinical team members and additional components of interventions that were done by the design of the intervention on top of the usual care provided to the control group for the respective article.For articles where the control group received usual care and additional care such as physical therapy sessions, we considered the roles and intervention components that were added on top of the control.Different clinical team member roles, as well as intervention components, were then categorized based on if they showed a clinically meaningful improvement in PROs compared to the control group in their respective studies.We used this to extrapolate results and recommendations to improve perioperative cancer care from these sparse studies.To ensure the accuracy and reliability of the synthesis, all intervention components extrapolated were discussed and modified through an interactive process with the entire team.The roles and intervention components were defined as follows: • Common roles = Roles taken on by the clinical team members during the intervention [33].
• Group education = Formal educational sessions where groups of patients got together to learn from the healthcare team [34].
• Patient/caregiver education = One on one education with the patient without a formal large group education session [35,36].
• Clinical follow-up = Standard follow-up with patients where symptoms are assessed, advice was given, and any questions are answered.The primary purpose of the follow-ups was not to solely educate the patients [37].
• Contact with patient throughout intervention = Contact throughout the intervention means that the clinical team member met with the patient in some capacity at least two different times throughout the intervention.
• Team structures = Who was part of the team, their roles, and their responsibilities.
• Team processes = Any form of communication/ collaboration that occurred with the interdisciplinary healthcare team.(eg.whether they had consistent meetings, ways they communicated, etc. ..) [38].
• Consistent communication = Consistent communication includes any communication/ collaboration processes that were set up among the interdisciplinary healthcare team.This included having consistent meetings and meeting with other team members at least two different times throughout the intervention.
• Referrals = The clinical team member directed the patient to other professionals such as physicians, other members of the interdisciplinary healthcare team, physiotherapists, psychologists, and nutritionists.
• Caregiver involvement = Caregivers included family members, friends, or surrogate decision makers who were somehow included in the intervention [39].

Literature selection
In total, 8,020 titles/abstracts were screened based on the inclusion and exclusion criteria.472 full-text articles were then screened for eligibility as shown by Fig 1 .We included 34 total studies in our review , of which 31 reported a clinically meaningful improvement in at least one PRO [40, 42-44, 46-58, 60-73].The included articles are summarized in Table 2 and Appendix S4 (S1 File).The studies reported 15 different PROs, as shown in Appendix S5 (S1 File).Appendix S5 (S1 File)also provides the ranges for the included PROs that determine MCID based on the most recent published data available.Team structures varied vastly across the interventions, wrangling from a nurse and physician team [40,45,50,54,56,57], a nurse and another member of the interdisciplinary healthcare team [43,52,60,66], and teams including three or more interdisciplinary healthcare team members [41, 42, 44, 47-49, 55, 61, 63, 64, 71].Team processes included consistent communication within the interdisciplinary healthcare team at multiple different points in time [40,44,45,51,56,62,64,67,71].Intervention components included clinical team members roles of group education, patient/caregiver education, and clinical follow-up, contact with the patient throughout the intervention, and caregiver involvement.Three studies included advanced practice providers (one article with advanced practice nurses and two articles with nurse practitioners) [43,44,55], nine studies included clinical nurse specialists

Common roles
Common roles taken on by the clinical team members throughout the interventions included group education, patient/caregiver education, and clinical follow-up.The roles, interventions, and PROs are summarized in Table 3.The education roles revolved around providing patients with more information regarding their diagnosis, potential complications, pain management,   relaxation techniques, exercise/diet, psychological support, and preventing cancer in the future.A total of eight studies included educational sessions [40, 44, 48, 60-62, 65, 66] and eight studies included individually educating patients [41,43,46,47,52,58,69,71], of which only one study did not report a clinically meaningful improvement in at least one PRO.The remaining eighteen studies had clinical follow-up as part of their intervention and eleven of these had a clinically meaningful improvement in at least one PRO [42, 45, 49-51, 53-57, 59, 63, 64, 67, 68, 70, 72, 73].Interventions with follow-ups may be associated with positive clinical effects on PROs if they included support for a patient's physical, emotional and mental health, psychosocial and spiritual support, and symptom relief.
Common roles of advanced practice providers.All three articles that included advanced practice providers in the intervention, regardless of the specific role they performed, were associated with an improvement in PROs compared to the control group in the respective articles [43,44,55].Koet  Common roles of nursing team members.The roles taken by clinical nurse specialists were distributed evenly with three articles utilizing interventions where the clinical nurse specialists led educational sessions [40,48,60], three articles providing patient/caregiver education [41,46,47], and three articles with clinical follow-up [42,45,49].Four articles included registered nurse roles of leading educational sessions [61,62,65,66], while four articles included registered nurse roles of patient/caregiver education with the patient [52,58,69,71], and fourteen articles included registered nurse roles of following up with the patient [50,51,53,54,56,57,59,63,64,67,68,70,72,73].Across the studies, there was heterogeneity regarding when the intervention began in the perioperative period relative to the date of surgery, as shown in Table 2.

Contact with patient throughout intervention
In studies where clinical team members maintained contact with patients for over six months throughout the intervention, there was a positive impact on PROs.Twenty-nine of the included studies involved nurse contact with the patient for more than one week [40-43, 45-50, 53, 54, 56-64, 66-73].Seventeen of these studies used telephone calls to maintain contact with the patient [40-43, 46-49, 53, 56-59, 63, 64, 67, 72] and three of the studies based in China also used WeChat [50,57,72].There was no significant difference between the different platforms for clinical follow-up, whether it was in-person, telephone, or any other modality, suggesting that the general act of contacting the patient throughout the intervention may contribute to improving patient quality of life [40-43, 46-50, 53, 56-59, 63, 64, 67, 72].The frequency of contact varied across the studies with some interventions having contact every few days, weekly, monthly, every few months, and even yearly.Timing of the clinical team member contact with the patient also varied across the studies in the perioperative period.One study conducted the intervention prior to the surgery [44], twenty-six studies conducted the intervention only after the operation was completed [41-43, 45-49, 51-53, 55-64, 66, 68-70, 73], and seven studies ran their intervention before and after the surgery [40,50,54,65,67,71,72].

Team structures
Team structures in the intervention arm varied across the 34 different studies.Six studies had a nurse and physician team structure [40,45,50,54,56,57] and five of them had improvements in PROs.Four studies had a nurse and another member of the interdisciplinary healthcare team [43,52,60,66] and eleven studies had three or more interdisciplinary healthcare team members [41, 42, 44, 47-49, 55, 61, 63, 64, 71].Thirteen of the studies only had the nurse as part of the intervention [46, 51, 53, 58, 59, 62, 65, 67-70, 72, 73].There are not enough included studies, and not enough information regarding team structures in the included studies to draw conclusions about the most effective team structures in improving PROs in perioperative cancer care.

Team processes
Consistent communication was another component of the interventions that was associated with an improvement in PROs.Nine of the studies included communication within the interdisciplinary healthcare team at multiple different points in time [40,44,45,51,56,62,64,67,71].This included working together to create a training session prior to implementing the intervention together, coordinating with each other throughout the intervention, or meeting with a interdisciplinary team on a frequent basis.Eight of these studies were correlated with improved PROs [40,44,51,56,62,64,67,71].
Nine of the studies included referrals as a form of communication, and this involved referrals to physicians, the interdisciplinary healthcare team, physiotherapists, psychologists, and nutritionists [41-43, 46-49, 53, 55, 57].These referrals took place throughout the intervention and were often due to the nurses identifying a factor that could improve the patient's quality of life through referrals.Eight of the interventions that included referrals were associated with an improvement in at least one PRO.

Caregiver involvement
Involvement of the patient's caregivers may be associated with an improvement in PROs compared to the control group of the respective studies.Caregiver involvement is pertinent because it serves as a way to define quality of care since in the case of serious illness or palliative populations, the patient themselves may have decreased decision making capacity and engagement of the family or caregiver ensures the patient's wishes are respected.Twelve studies included the patient's caregivers, families, social support systems, and/or friends in the intervention and eleven of these studies had at least one clinically significant improvement in PROs [40, 43, 44, 48-50, 58, 59, 64, 66, 70, 73].Three of the studies allowed caregivers to participate in the educational sessions [40,44,48] while some interventions facilitated communication with the caregivers about management strategies and other interventions encouraged caregivers to accompany the patient as much as possible or serve as interpreters.

Discussion
Multiple randomized controlled trials have evaluated the effect of interdisciplinary team interventions on PROs in the perioperative period, however, the studies have notable heterogeneity.Since no included articles had an overall high risk of bias, all studies were of high quality and thus minimize potential bias in the conclusions drawn from this systematic review.Among the RCTs included, there were common intervention components that might drive a positive clinical effect in PROs.While the specific roles of clinical team members varied across interventions, common roles included leading group education, patient/caregiver education, and clinical follow-up.Topics for group education included information regarding the diagnosis, relaxation techniques, exercise/ diet, psychological support, and preventing cancer in the future, while follow-up topics included support for a patient's physical, emotional and mental health, psychosocial and spiritual support, and symptom relief.Continuous contact with the patients throughout the intervention (e.g.multiple telephone and in-person follow-ups before and after the surgery) [40] may have a positive impact on PROs in the perioperative period; a majority of included articles included over six months of patient contact.Other components of interventions that may show improvements in PROs were increasing consistent communication and collaboration among the interdisciplinary healthcare team and involving caregivers to support the patient.
In the included studies, clinical team members expanded their roles by facilitating group education, patient/caregiver education, and patient clinical follow-up.Studies have shown that incorporating trained nurses into care processes, with surgeons, can improve cancer care experiences and patient satisfaction determined by PROs [75,76].The actual content of the education or follow-up done by the nurses varied vastly and the expansion of the clinical team member role itself serves as a component of interventions that may improve PROs.In the group setting, outcomes in the QLQ-c-30, Profile of Mood States, and MACL were improved, which may be attributed to patients being in the physical presence of each other and providing reassurance and camaraderie, accumulating knowledge together, and asking questions [40, 44, 48, 60-62, 65, 66, 77].For example, Koet et al., 2021 demonstrated a statistically significant difference in the QLQ-C30 at the one month follow up between the intervention arm (mean = 72.1)and the control arm (mean = 63.9)[44].The model of patient/caregiver education and clinical follow-up has been well-established in cancer care and personalizes the patient education experience based on their own recovery and allows patients privacy for uncomfortable topics [78][79][80].Due to limited resources and time for surgeons, clinical team members can take on an expanded role in cancer care to conduct patient/caregiver education or clinical follow-up with the patients [81][82][83].
This narrative systematic review adds to the current knowledge of how team based interventions improve PROs in cancer care, which supports potentially expanding the healthcare team by involving additional clinical team members to share the care alongside physicians.Articles that include interventions that leverage clinical team members may not necessarily use the terms "team" or "teamwork" or "teaming" to define the interactions among the clinical team members and the rest of the interdisciplinary healthcare team.In our abstraction form, we captured both formal team based interventions as well as dynamic teaming processes.Broadening the definition of teamwork to also include teaming was necessary so that we could include more articles that leveraged interdisciplinary contributions, which allowed us to demonstrate sharing care with multiple clinical team members is a common intervention feature among articles with improved patient-reported outcomes in perioperative cancer care.
In light of the high rates of physician burnout and limited time and resources for physicians, advanced practice providers can help share the care by serving as full time equivalents (FTEs) for physicians [6][7][8]81].Inclusion of advanced practice providers has been shown to reduce overall cost and provide support for physicians [82].Given the well-known workforce constraints for palliative care in cancer, advanced practice providers are an ideal alternative to maintain quality of care while considering overall healthcare expenditure [83].Oncology advanced practice providers can lead follow-up visits and educational sessions for patients in addition to administrative and clinical responsibilities, making this a viable opportunity specifically in the context of perioperative cancer care [84].
Clinical team members contact with patients, and communication with the rest of the interdisciplinary healthcare team at multiple times, are both key components of interventions that may be associated with improved PROs for patients with cancer in the perioperative period.Longitudinal patient contact is seen in cancer care contexts, where long-term patient contact with physicians or other healthcare professionals is associated with improved patient care [85][86][87].In almost all the included perioperative studies, longitudinal patient contact was seen, but was especially exemplified by Mertz et al., 2017 where there were no improvements in patient reported outcomes at six months, but there were clinically and statistically significant improvements in the intervention group at twelve months [46].In the literature, several studies have shown that using consistent communication within the healthcare team can be an effective part of interventions for treating patients with different types of cancer in different stages of treatment [5,88,89].Longitudinal follow-up and effective communication among the healthcare team, with referrals to healthcare team members, may be used to improve the quality of life for patients with cancer in the perioperative period [90].
In cancer care, many studies have been provider focused rather than involving patient/ caregiver input, so, including caregivers in interventions, and utilizing their input in developing interventions serves as an opportunity for improvement [91].Involvement of the patient's caregivers in ten of the included articles came in different forms, differing on who was included and how they contributed to the intervention [40, 43, 44, 48-50, 58, 59, 64, 66, 70, 73].Studies focusing on cancer care have shown the effectiveness of involving caregivers to allow for shared decision making to improve mental health and resilience, which is consistent with improvements in the QLQ-c30, Stoma Self-Efficacy Scale, HADS, and MACL PROs [92,93].Including caregivers in cancer interventions has also translated to improved patient satisfaction, suggesting it may be a worthwhile component to include in the treatment of patients with cancer in the perioperative period [94].
Our study can be considered in light of the following limitations.The incorporation of advanced practice providers in the interdisciplinary healthcare team is recent and only three articles that had an intervention with advanced practice providers were included from a limited body of literature.We anticipate an increasing number of publications with interventions that include advanced practice providers.The patient reported outcomes included were heterogeneous and thus a meta-analysis or further synthesis is not possible.Further, PROs hold the bias that patients may have their own individual reference points for answering the questions [95].Our abstraction form did not capture the type of surgeon, which may be relevant in understanding PROs in different perioperative contexts.Furthermore, the search strategy itself, and the screening process, may have missed certain articles.The included studies were heterogeneous in nature, which did not allow for statistical analysis, thus limiting the conclusions formed in this study.Finally, the included studies did not provide sufficient information in the manuscript regarding the purpose of surgeon interaction with the patient during the perioperative period (communicate the purpose and expect results of surgery, identify patients who are appropriate for surgery, optimize patients for surgery to minimize risks, or identify and manage complications postoperatively), which may have added an additional layer of understanding.Future studies could consider the type of surgeon and the purpose of surgeon interaction with the patient during the perioperative period to better understand if differences in these factors may impact PROs.

Conclusion
By broadening the definition of teamwork to include teaming, we were able to build upon the current knowledge of team-based interventions, particularly for improving PROs in perioperative cancer care.Our review demonstrated common structures and processes across interventions that impacted PROs in the perioperative period.These included expanding the roles of any clinical team members (advanced practice providers, nurse practitioners, or registered nurses) to include either group education, patient/caregiver education or clinical follow-up since they all demonstrated improved PROs.Other intervention components included longitudinal follow-up for longer than six months, increasing consistent communication among the interdisciplinary healthcare team, and involving caregivers in any capacity.The intervention components found in this study can be leveraged in efforts to improve perioperative cancer care based on the resources available and the specific needs of the patients.In addition, different types of surgeons have different practices, workflows, and practice cultures.Interventions that work for one practice culture may need to be adapted to translate into other practice cultures.In conjunction with results of design focused, formative interviews with palliative care teams and surgeons, the evidence synthesized through this systematic review will be used to build an interdisciplinary teaming intervention [96].Future interventions might prioritize expanding the roles of clinical team members to include educating patients, engaging the patient's caregiver, and ensuring sufficient follow-up towards improving quality for patients in the perioperative period.
[40-42, 45-49, 60], and 23 studies included registered nurses [50-59, 61-73] (Wallen et al., 2012 included both an advanced practice provider and a registered nurse in their intervention); all three studies with advanced practice providers reported a clinically meaningful improvement.No included studies had an overall high risk of bias as per the Cochrane Risk of Bias tool.

Fig 1 .
Fig 1. PRISMA flowchart [74].https://doi.org/10.1371/journal.pone.0294599.g001 et al., 2021 designed an intervention in which nurse practitioners gave PowerPoint presentations during an educational class to teach patients about their diagnosis, therapy, hospitalization, potential side effects, functional implications and to provide psychoeducation to help patients cope with cancer.The other article that utilized nurse practitioners (Wallen et al., 2012) ensured follow-up with the patients regarding physical symptoms, and emotional/ spiritual distress as part of their intervention.In McCorkle et al., 2009, advanced practice nurses educated patients on symptom management, diagnosis/ treatment, and provided support via counseling.